Synaptic pharmacology in the turtle accessory optic system

Abstract

The accessory optic system of the turtle (the basal optic nucleus, BON) receives both excitatory and inhibitory inputs that are direction-sensitive. When the dorsal midbrain is ablated, only the monosynaptic direction-sensitive input from the retina to the BON remains. To better understand the central visual processing performed by the accessory optic system, this study identifies the neurotransmitters and their receptors that mediate the synaptic excitation and inhibition of BON cells. We used a reduced in vitro turtle brainstem preparation in which the two eyes and brain were isolated pharmacologically. Patch recordings were made on BON neurons while drugs were applied to the brain, with the eyes bathed in control media and either exposed to visual pattern motion or subjected to electrical stimulation. An antagonist of the AMPA (alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) subtype of glutamate receptor applied within the brain chamber blocked the visual responses. In response to electrical stimulation both excitatory and inhibitory synaptic events were blocked in BON cells, presumably by blocking direct excitation by retinal ganglion cell axons in the BON and indirect excitation of inhibitory interneurons elsewhere in the brainstem. An NMDA receptor antagonist was ineffective, even when the response was measured in a BON cell depolarized in Mg(2+)-free media. A GABA(A) receptor on the BON cell mediates the inhibitory responses to retinal stimulation. Injection of lidocaine into the contralateral eye caused an increase in spontaneous inhibitory post-synaptic potentials (IPSPs), suggesting that a tonic retinal output exists that reduces brainstem inhibition of BON cells. Also, there may be tonic inhibition of an excitatory path to BON neurons from within the brainstem, because bicuculline increased spontaneous excitatory post-synaptic potentials (EPSPs) observed in a BON cell without retinal input. These results indicate that the BON is a site of complex visual processing of competing visual signals and provide insight into how an interaction of excitation and inhibition creates a retinal slip signal in the accessory optic system.

The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function

“…The importance of such an arrangement is that it allows 1) enhanced spatial coding (enhanced receptive fields) by convergence many retinal ganglion cells directly on the AOS neuron and indirectly through retino-NLM-nBON projections, 2) gain enhancement on the AOS neurons, and/or 3) sensory processing or tuning through a convergence of excitatory and inhibitory inputs (Ariel and Kogo, 2001). Further pharmacological studies on the turtle AOS revealed that of the converging, direction-selective, inhibitory/excitatory inputs to the nBOR, the inhibitory inputs are blocked by bicuculline mediated by the retinal-pretectal connections acting upon GABA (A) receptors located on the nBOR neurons, whereas the excitatory input is from retinal glutaminergic retinal afferents, given that retinal excitation of the nBOR was blocked by an antagonist of the AMPA (alphaamino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) glutamate receptor subtype (Kogo and Ariel, 2002). The likely source of direction-selectivity of NOT/DTN neurons remains their retinal input from excitatory, on-center, direction-selective retinal ganglion cells (Oyster et al, 1972;Hoffmann and Stone, 1985.…”

Influence of the behavioural context on the optocollic reflex (OCR) in pigeons (Columba livia)

“…Ariel and Kogo (2001), using a turtle brain stem preparation with the eyes attached, observed that visual stimuli provoked both excitation and inhibition of the nBOR neurones. These neurones also probably receive a tonic activation and inhibition from the retina and other cells (Kogo et al, 2002). The retinal slip signal may be due to these competing excitatory and inhibitory visual inputs.…”

Shunting Inhibition in Accessory Optic System Neurons

“…The accessory optic system receives direct excitatory input from the retina (Kogo and Ariel 1997;Zhang and Eldred 1994) and indirect inhibitory input from the pretectum (Kogo et al 2002). Both excitatory and inhibitory responses to pattern motion on the contralateral retina are direction-sensitive (Ariel and Kogo 2001).…”

“…The excitatory response from the retina is mediated entirely by AMPA receptors, while pretectal stimulation evokes an inhibitory response that is Cl Ϫ mediated and blocked by a GABA A receptor antagonist (Kogo et al 2002). The time course of nonlinear interactions of coincident excitation and inhibition were evaluated during whole cell patch recordings in the intact turtle brain stem.…”

“…The experiments here investigate synaptic integration on a membrane level in a system for which it has been shown that natural stimuli evoke simultaneous excitatory and inhibitory inputs onto the same cell (Ariel and Kogo 2001). These cells in the accessory optic system relay retinal slip information to the cerebellum and numerous brain stem nuclei for compensatory head and eye movements (Brecha and Karten 1979;Simpson 1984).The accessory optic system receives direct excitatory input from the retina (Kogo and Ariel 1997;Zhang and Eldred 1994) and indirect inhibitory input from the pretectum (Kogo et al 2002). Both excitatory and inhibitory responses to pattern motion on the contralateral retina are direction-sensitive (Ariel and Kogo 2001).…”